Citizen scientists contributing to alien species detection: the case of fishes and mollusks in European marine waters

Abstract

Citizen science (CS) expands the spatial and temporal scale of alien species records. As such, it has been recognized as a complementary tool in alien species management and large‐scale biodiversity conservation. The present study assessed the contribution of CS to the recording of marine alien fishes and mollusks in European marine waters by reviewing data available through the European Alien Species Information Network, portals, public databases, and scientific literature. In total, 8,513 CS records were retrieved, following a filtering procedure, and assessed. A positive relationship was found between CS records and time, with most of records being reported during the last decade. The presence of alien fishes was recorded by citizens in seven out of nine Marine Strategy Framework Directive (MSFD) subregions, while mollusks were recorded in all MSFD subregions. Most of the CS records of fishes were reported in the Mediterranean Sea and mostly in the Aegean‐Levantine Sea. Conversely, most of the CS records of mollusks were reported in NE Atlantic Ocean, mostly in the Greater North Sea. A key finding is that eight species were documented for the first time in European marine waters and other three were recorded outside of their known distribution range. The majority of CS reporting was funneled through scientific surveys in which the nature of CS participation was limited to data collection only. The main categories of citizen scientists included school children, students, divers, naturalists, and various volunteers. Overall, 88.5% of marine alien fishes and mollusks recorded by citizens were validated by taxonomical experts, and only 15.8% out of the validated records were supplemented with pictures. CS can contribute to early detection and enhance cost‐effectiveness of monitoring and surveillance programs regarding alien species in European seas. Still, it requires proper scientific support and adequate validation tools mechanisms.

Introduction

Marine invasive alien species (IAS) constitute one of the four greatest threats to the world's oceans at local, regional, and global scale (IMO 2000–2004). They have been recognized as one of the most common drivers of biodiversity loss (Bellard et al. 2016). IAS can modify habitats, change species composition of ecosystems, affect food-web properties and ecosystem processes, impede the provision of ecosystem services, impact human health, and cause substantial economic losses (Wallentinus and Nyberg 2007, Molnar et al. 2008, Katsanevakis et al. 2014).

European seas host the highest number of marine alien species, the vast majority of which are native to the Western and Central Indo-Pacific (Tsiamis et al. 2018). For this reason, marine IAS are targeted by European Union (EU) policy, such as the EU Regulation on the prevention and management of the introduction and spread of invasive alien species (EC 2014, IAS Regulation), and the Marine Strategy Framework Directive (MSFD). The IAS Regulation requests EU Member States (MSs) to “carry out a comprehensive analysis of the pathways of unintentional introduction and spread of IAS in their territory and identify the pathways, which require priority action (priority pathways), because of the volume of species or of the damage caused by the species entering the Union through them” (EC 2014, Art.13.1). The MSFD requires EU MSs to consider alien species (=non-indigenous species) when developing their marine management strategies (EC 2008, 2010, 2017).

There is a wide international consensus that holistic, preventive, multi-vector pathways-based management is an absolute priority to effectively combat marine alien species (Ojaveer et al. 2018). Therefore, establishing cost-effective monitoring plans for preventing and reducing the risk of alien species introduction is crucial, and citizen science (CS) is one of the possible initiatives (Pocock et al. 2017, Mannino and Balistreri 2018).

Citizen science, the engagement of non-professionals in scientific investigations (Miller-Rushing et al. 2012), aims to create or increase datasets on temporal and spatial scales (Dickinson et al. 2012), and to educate members of the public (Bonney et al. 2009a) contributing to the growth of CS programs in several disciplines (Jordan et al. 2015). For example, CS is used to tackle key questions in ecology and conservation, including spatial and macro-ecology, management of threatened and invasive species, and biodiversity monitoring (Kobori et al. 2016). CS allows for large-scale, both temporal and spatial, biodiversity monitoring (Chandler et al. 2016) and the detection of long-term ecosystem changes (Gouraguine et al. 2019). Furthermore, CS has the potential to increase the scientific knowledge on marine alien species, given the huge number of records of species that can be obtained (Johnson et al. 2020) through the large-scale monitoring with the involvement of citizens (e.g., tourists, fishers, divers), also increasing the chance for early detection (Myers et al. 2000, Bax et al. 2001, Thomas et al. 2017). In this respect, CS can complement the EU MS official surveillance in detecting the occurrence of new IAS under the IAS Regulation (Cardoso et al. 2017).

Citizen science initiatives have expanded worldwide during the last decades as a result of the development of information and communications technology (ICT) tools (Miller-Rushing et al. 2012, Cappa et al. 2016). The internet and the increasing popularity of technology, including smartphones, have fueled the interaction between citizen volunteers and professional scientists. Data, also including alien species records, are increasingly generated through web interfaces, such as iNaturalist, Natusfera, and iSpot, or smartphone-based CS applications, such as the JRC app “Invasive Alien Species Europe,” “That's Invasive!” and the IUCN app “MedMIS” (Dickinson et al. 2012, Starr et al. 2014, Adriaens et al. 2015, Schade et al. 2019). In a recent review, Johnson et al. (2020) recorded 26 CS initiatives collecting alien species data using ICT, while in the last decade, hundreds of biodiversity-related CS projects, many of which collect alien species observations, were initiated (Theobald et al. 2015). Currently, CS has widely been recognized as an effective tool to expand the scale of alien species data collection and monitoring (Mannino and Balistreri 2018), although novel training methods of the participants that can be remotely administered are needed and have already started to be employed by various projects (Crall et al. 2011, Starr et al. 2014, Roy et al. 2018).

In the present study, we assessed the contribution of citizens to the recording of alien fishes and mollusks in European marine waters by conducting a thorough review of CS data hosted in networks, portals, public databases, and scientific literature. For each CS record, a detailed description is provided, including its taxonomic classification, geographical origin, year of record, and level of validation. In addition, a comparison of the CS records with the existing scientific knowledge on marine alien fishes and mollusks occurrences in Europe is performed.

Methods

Citizen science records of marine alien fishes (Phylum: Chordata, Class: Actinopterygii) and mollusks (Phylum: Mollusca, Classes: Bivalvia, Cephalopoda, and Gastropoda) in European marine waters were investigated. The methodological steps followed for this purpose are shown in Fig. 1. Following the conceptualization and the methodological design of this work, CS records were retrieved after an in-depth use of the pan-European inventory of alien species, namely, the European Alien Species Information Network (EASIN: https://easin.jrc.ec.europa.eu/; Katsanevakis et al. 2012, 2015), which is the EU official information system supporting the implementation of the IAS Regulation. The EASIN Geodatabase (Deriu et al. 2017) includes alien species data (including CS data) coming from a network of Data Partners (Appendix S1: Table S1). Among these datasets, particular attention was paid to the CS records retrieved from the Global Biodiversity Information Facility (GBIF: https://www.gbif.org/). GBIF hosts a high number of CS records from all over Europe, and it is the largest online platform that integrates digitized collection and survey data about species occurrence and distribution (Beck et al. 2014). CS records of marine alien fishes and mollusks in European marine waters were further enriched by checking additional portals including CS records, such as iNaturalist (https://www.inaturalist.org/), Natusfera (http://natusfera.gbif.es), and the databases of Non-Governmental Organizations such as SEAWATCHERS (http://www.seawatchers.org/que-es.php) and Spot the Alien Fish (http://www.aliensmalta.eu/). These portals were highly relevant because of their active communities and well-established practices. Finally, relevant scientific literature that includes CS records on marine alien species was checked (e.g., Zenetos et al. 2013, Kousteni et al. 2019).

Fig. 1. Graphical representation of the procedure followed in the present study from the methodological design to the dissemination of results.

The review of the aforementioned data sources resulted in 34,954 individual records of alien fishes and mollusks in Europe by 18 March 2019. A filtering procedure applied resulted in 8,513 records meeting the following criteria: (1) Geographical origin: Only alien species were taken into consideration. Cryptogenic species, that is, species with no definite evidence on their native or alien status due to unknown origin and crypto-expanding species with some evidence on their non-indigenous status but with uncertainty due to unclear mode of introduction from native range: natural spread vs. human mediated (Zenetos et al. 2020); questionable species, that is, species with insufficient information or new entries not verified by experts or species with unresolved taxonomic status, were not included in this study; (2) ecosystem type: Marine species were taken into consideration. Oligohaline (estuarine) and freshwater species were excluded from the analysis; (3) Country of record: All records represented species reported only from EU countries and the United Kingdom. Specifically, the geographical scope of our study was the MSFD European marine water regions (Mediterranean Sea: Adriatic Sea, MAD; Aegean-Levantine Sea, MAL; Ionian Sea and the Central Mediterranean Sea, MIC; Western Mediterranean Sea, MWE; NE Atlantic Ocean: Bay of Biscay and the Iberian Coast, ABI; Celtic Seas, ACS; Greater North Sea, ANS; Black Sea, BLK; and Baltic Sea, BAL). The Macaronesia region was excluded; (4) Data provider type: Only records reported by citizens were taken into consideration.

Following the filtering procedure, detailed information was retrieved for each marine alien fish and mollusk taxon recorded by CS including: (1) the taxonomic classification (Kingdom, Phylum, Class, Order, Family, and Species) following WoRMS (2021), (2) subregional sea of record based on the MSFD context, (3) country of record, (4) year of record, (5) type of dataset source, (6) nature of CS participation according to Jordan et al. (2015), and (7) level of data validation. For the description of the level of validation of each CS record, we followed the following steps: (a) The records were classified into two categories (validated vs. non-validated), (b) the means of validation was recorded, (c) CS records supplemented with pictures were indicated, and (d) for the picture-provided CS records with an accessible web link, the taxonomic classification was cross-checked by our scientific team of experts. The finalized dataset was analyzed to examine the geographical distribution of CS records per taxon, by MSFD subregion and country, and to estimate the level of validation per taxon. Finally, all CS records were compared with the existing known distribution of the marine alien fishes and mollusks in Europe by using the EASIN Geodatabase and scientific literature. The CS records that fell outside the known alien range of the investigated alien species across Europe were highlighted.

Results Description of CS records

In total, 8,513 CS records of marine alien fishes and mollusks were recorded in European marine waters by 18 March 2019, with most of them being reported from 2007 to 2018 (Figs. 2, 3). The observed CS records belonged to Actinopterygii (N = 1,002) and Mollusca (N = 7,511) corresponding to 68 and 72 species, respectively (Table 1). Among fishes, the highest numbers of CS records were found for Lagocephalus sceleratus (24.85%), Pterois miles (12.57%), Fistularia commersonii (11.18%), Siganus luridus (9.38%), Stephanolepis diaspros (7.19%), Siganus rivulatus (5.69%), Sargocentron rubrum (4.59%), and Torquigener flavimaculosus (4.59%). Among mollusks, the Class Gastropoda was the most highly reported in terms of number of records (51.63%) and number of species (N = 65.28%). The two highest percentages of CS records of mollusks belonged to the gastropod Crepidula fornicata (44.87%) and the bivalve Magallana gigas (23.10%). The bivalves Petricolaria pholadiformis (10.37%) and Mya arenaria (10.08%) were also highly reported. A single CS record was found for 28 and 20 marine alien fishes and mollusks, respectively. A complete description of the CS records of marine alien fishes and mollusks is presented for each species, country, and MSFD marine subregion in Data S1: CS records.

Fig. 2. Total number of citizen science records of alien fishes and mollusks in European marine waters per MSFD subregion (Mediterranean Sea: MAD, Adriatic Sea; MAL, Aegean-Levantine Sea; MIC, Ionian Sea and the Central Mediterranean Sea; MWE, Western Mediterranean Sea; Black Sea, BLK; NE Atlantic Ocean: ABI, Bay of Biscay and the Iberian Coast; ACS, Celtic Seas; ANS, Greater North Sea; BAL, Baltic Sea).

Fig. 3. Time evolution in the total number of citizen science (CS) records of alien fishes and mollusks in European marine waters per MSFD subregion (Mediterranean Sea: MAD, Adriatic Sea; MAL, Aegean-Levantine Sea; MIC, Ionian Sea and the Central Mediterranean Sea; MWE, Western Mediterranean Sea; Black Sea, BLK; NE Atlantic Ocean: ABI, Bay of Biscay and the Iberian Coast; ACS, Celtic Seas; ANS, Greater North Sea; BAL, Baltic Sea). CS records in terms of number of individuals (solid lines) and number of species (dashed lines with marker) are presented for alien fish (black color) and mollusks (red color) separately. CS records in 2019 were excluded from the graph given their short-time coverage.

Table 1 Number of citizen science (CS) records and species of alien fish (Phylum: Chordata, Class: Actinopterygii) and mollusks (Phylum: Mollusca, Classes: Bivalvia, Cephalopoda, and Gastropoda) in European marine waters.

Taxon	CS Records	Species
Chordata	1,002	71
Actinopterygii	1,002	71
Atheriniformes	1	1
Beloniformes	7	2
Beryciformes	50	3
Clupeiformes	1	1
Perciformes	318	52
Scorpaeniformes	132	3
Syngnathiformes	112	1
Tetraodontiformes	381	8
Mollusca	7,511	72
Bivalvia	3,540	23
Arcida	3	2
Cardiida	2	2
Myida	757	1
Mytilida	39	4
Ostreida	1,795	6
Pterioida	17	1
Venerida	927	7
Cephalopoda	93	2
Myopsida	91	1
Octopoda	2	1
Gastropoda	3,878	47
Aplysiida	40	2
Caenogastropoda	48	9
Cephalaspidea	82	7
Cycloneritimorpha	11	1
Lepetellida	11	1
Littorinimorpha	3,507	6
Neogastropoda	67	7
Nudibranchia	77	9
Pleurobranchida	1	1
Sacoglossa	31	2
Trochida	1	1
Pylopulmonata	2	1

Geographical distribution of records

Alien fishes were recorded by CS in seven out of nine MSFD subregions in 11 EU MS (Figs. 4a, 5a). Mollusks were recorded in all nine (Macaronesia excluded) MSFD subregions in 20 EU MS and the United Kingdom (Figs. 4b, 5b). In the case of fishes, the highest number of CS individual records was found in the Mediterranean Sea, mainly in MAL (65.87%), coming mainly from Greece (56.19%) and Cyprus (16.67%), while the lowest number of records was found in the NE Atlantic, including ANS and ABI (0.10% each). No CS records of alien fishes were found in ACS and BLK (Figs. 4a, 5a). Regarding alien mollusks, the highest number of CS records came from NE Atlantic, from ANS (69.50%) and ACS (16.60%), and specifically the United Kingdom (47.14%), the Netherlands (17.47%), and Germany (10.57%), while very few records were reported by CS in the other MSFD subregions (Fig. 3). Among mollusks, Bivalvia were recorded by CS in all MSFD subregions, Gastropoda were recorded in all MSFD subregions except BAL, and Cephalopoda were recorded only in the Mediterranean Sea mostly in MAL (97.85%). The two highest percentages of CS records of Bivalvia and Gastropoda were found in NE Atlantic, in the MSFD subregions ANS (71.61% and 69.24%, respectively) and ACS (15.31% and 18.18%, respectively) (Fig. 4b). Bivalvia were primarily recorded in the Netherlands (28.67%), but many records were also found in the United Kingdom (21.55%), Germany (18.70%), and Belgium (16.55%). On the other hand, Gastropoda were mostly recorded in the United Kingdom (71.63%) with lower contributions from other countries (0.03–7.53%), and Cephalopoda mostly in Greece (90.32%) (Fig. 5b).

Fig. 4. Percentage (%) of citizen science (CS) individual records of alien fishes (a) and mollusks (b) in European marine waters per MSFD subregion (Mediterranean Sea: MAD, Adriatic Sea; MAL, Aegean-Levantine Sea; MIC, Ionian Sea and the Central Mediterranean Sea; MWE, Western Mediterranean Sea; Black Sea, BLK; NE Atlantic Ocean: ABI, Bay of Biscay and the Iberian Coast; ACS, Celtic Seas; ANS, Greater North Sea; BAL, Baltic Sea).

Fig. 5. Percentage (%) of citizen science (CS) individual records of alien fishes (a) and mollusks (b) in European marine waters per EU Member State (BE, Belgium; BG, Bulgaria; CY, Cyprus; DE, Germany; DK, Denmark; EE, Estonia; EL, Greece; ES, Spain; FI, Finland; FR, France; HR, Croatia; IE, Ireland; IT, Italy; LV, Latvia; LT, Lithuania; MT, Malta; NL, The Netherlands; PT, Portugal; RO, Romania; SE, Sweden; SI, Slovenia) and the United Kingdom (UK).

The majority of marine alien species of fish reported through CS were observed in the Mediterranean Sea, and specifically in MAL (N = 45), with 41 and 27 species reported in Greece and Cyprus, respectively, followed by MIC (N = 23), MWE (N = 10) and MAD (N = 11), while only one fish species was reported in ABI and BAL, and three species in ANS (Figs. 6a, 7a). The majority of marine alien species of mollusks was recorded in MAL (N = 48) followed by MWE (N = 19), ANS (N = 13), MIC (N = 9), MAD (N = 9), ABI (N = 8), and ACS (N = 7), while one species was reported in BAL and two species in BLK (Fig. 6b). The highest number of mollusk species was reported in Cyprus (N = 34), followed by Greece (N = 33), Spain (N = 13), Italy (N = 13), and France (N = 12), and fewer species were reported in the remaining countries (Fig. 7b).

Fig. 6. Number of species of alien fish (a) and mollusks (b) reported through citizen science in European marine waters per MSFD subregion (Mediterranean Sea: MAD, Adriatic Sea; MAL, Aegean-Levantine Sea; MIC, Ionian Sea and the Central Mediterranean Sea; MWE, Western Mediterranean Sea; Black Sea, BLK; NE Atlantic Ocean: ABI, Bay of Biscay and the Iberian Coast; ACS, Celtic Seas; ANS, Greater North Sea; BAL, Baltic Sea).

Fig. 7. Number of species of alien fish (a) and mollusks (b) reported through citizen science in European marine waters per EU Member State (BE, Belgium; BG, Bulgaria; CY, Cyprus; DE, Germany; DK, Denmark; EE, Estonia; EL, Greece; ES, Spain; FI, Finland; FR, France; HR, Croatia; IE, Ireland; IT, Italy; LV, Latvia; LT, Lithuania; MT, Malta; NL, The Netherlands; PT, Portugal; RO, Romania; SE, Sweden; SI, Slovenia) and the United Kingdom (UK).

First records and discrepancies in geographical distribution of marine alien fishes and mollusks reported by CS

Seven species of marine alien fish and one mollusk species were reported by CS for the first time in European marine waters (Table 2). All these records, except Chaetodon larvatus, Holocentrus adscensionis, Hyporhamphus affinis, and Pinctada margaritifera, were validated by taxonomic experts. Additionally, Lutjanus fulviflamma was reported for the first time in the Mediterranean Sea, Pinctada imbricata radiata was reported for the first time in the NE Atlantic Ocean, and Synanceia verrucosa was reported for the first time in France. Out of the three observed discrepancies, only Synanceia verrucosa was not validated and further research is needed for safer assumptions to be made.

Table 2 List of alien fishes and mollusks reported through citizen science in European marine waters that showed discrepancies in their known geographical distribution by 18 March 2019 (MSFD subregions: ABI, Bay of Biscay and the Iberian Coast; ANS, Greater North Sea; BAL, Baltic Sea; MAL, Aegean-Levantine Sea; MIC, Ionian Sea and the Central Mediterranean Sea; MWE, Western Mediterranean Sea; EU countries: CY, Cyprus; EL, Greece; DE, Germany; FR, France; MT, Malta; NL, The Netherlands; PT, Portugal).

Species	ABI	ANS	BAL	MAL	MAL	MIC	MWE
	PT	NL	DE	CY	EL	MT	FR
Phylum: Chordata
Order: Actinopterygii			1	3	5	2	2
Acanthurus gahhm (Forsskål, 1775)†,‡					1
Arothron hispidus (Linnaeus, 1758)§,‡				1
Cephalopholis hemistiktos (Rüppell, 1830)†,‡						1
Chaetodipterus faber (Broussonet, 1782)¶,‡					4
Chaetodon larvatus Cuvier, 1831†,‡							1
Holocentrus adscensionis (Osbeck, 1765)¶,‡				2
Hyporhamphus affinis (Günther, 1866)§,‡			1
Lutjanus fulviflamma (Forsskål, 1775)§,#						1
Synanceia verrucosa Bloch & Schneider, 1801§,||							1
Phylum: Mollusca
Order: Bivalvia	1	1
Pinctada imbricata radiata (Leach, 1814)§,††		1
Pinctada margaritifera (Linnaeus, 1758)§,‡	1

Notes:

Geographical origin and first records: †Western Indian; ‡First record in European marine waters; §Indo-Pacific; ¶Tropical Atlantic; #First record in the Mediterranean Sea; ||First record at country level; ††First record in the NE Atlantic Ocean.

Level of validation of CS records

The main categories of citizens reporting on marine alien fishes and mollusks in European marine waters included school children, students (16+), divers, non-professional naturalists, and various volunteers. The majority (78.80%) of CS records were reported by citizens that were involved in scientific surveys and were guided by experts. The nature of CS participation in these scientific projects was limited to data collection only. The remaining (21.20%) CS records were reported individually through various portals and scientific literature (Data S1: CS records, Metadata S1). In total, 19 different sources of CS records of marine alien fishes and mollusks in European waters were recorded, including Web-paged platforms, biodiversity databases, scientific projects, and publications. The geographical distribution of the different sources of CS records of alien fishes and mollusks is presented per MSFD subregion showing a higher activity in CS initiatives and reporting in ANS and MWE (Fig. 8).

Fig. 8. Number of datasets including records of alien fishes (a) and mollusks (b) reported through citizen science in European marine waters per MSFD subregion (Mediterranean Sea: MAD, Adriatic Sea; MAL, Aegean-Levantine Sea; MIC, Ionian Sea and the Central Mediterranean Sea; MWE, Western Mediterranean Sea; Black Sea, BLK; NE Atlantic Ocean: ABI, Bay of Biscay and the Iberian Coast; ACS, Celtic Seas; ANS, Greater North Sea; BAL, Baltic Sea). Detailed information about the different types of datasets considered in the present study is presented in Data S1: CS records, Metadata S1.

The majority of the CS records concerning both taxonomic groups were validated by experts (Fig. 9a). In the case of fishes, 971 out of 1,002 CS records were validated by taxonomic experts corresponding to 65 out of 71 species. The highest percentages of the validated CS records referred to L. sceleratus (25.54%), Siganus spp. (15.35%), P. miles (12.98%), F. commersonii (11.33%), and S. diaspros (7.42%). In the case of mollusks, 6,564 out of 7,511 CS records were validated by taxonomic experts corresponding to 70 out of 72 species. Most of the validated CS records came from the gastropod C. fornicata (48.78%) and the bivalve Mallagana gigas (23.20%), followed by P. pholadiformis (8.68%), M. arenaria (6.22%), and the rest of the species in lower (<2%) percentages.

Fig. 9. Percentage (%) of citizen science (CS) records of alien fishes (Phylum: Chordata, Class: Actinopterygii) and mollusks (Phylum: Mollusca, Classes: Bivalvia, Cephalopoda, and Gastropoda) in European marine waters that have been validated by taxonomic experts (a) and have also been provided with a picture (b).

Overall, 21.11% and 15.07% of the CS validated records of alien fishes and mollusks, respectively, were provided with pictures (Fig. 9b). In the case of fishes, the validated CS records with pictures corresponded to 52 species, mostly to P. miles (17.07%), Siganus spp. (16.10%), L. sceleratus (14.15%), and F. commersonii (11.71%). In the case of mollusks, the validated CS records with pictures corresponded to 61 species, mostly to the bivalve Mallagana gigas (32.15%) and the gastropod C. fornicata (30.64%).

Discussion

The efficient management of alien species requires, inter alia, the timely availability of updated high-quality data. This necessity combined with the growing threat posed by the introduction of marine alien species highlights the importance of CS research in documenting the distribution of introduced organisms in places and at scales that would otherwise not be possible (Dickinson et al. 2012, Mannino and Balistreri 2018).

Our study confirmed the significance of CS in recording marine alien taxa at both large and small geographical scale, a valuable knowledge that could improve the management activities toward marine invasions. According to a thorough review of CS data hosted in networks, portals, public databases, and scientific literature conducted by 18 March 2019, alien fishes were recorded by citizens in seven out of nine MSFD subregions and alien mollusks were recorded in all MSFD subregions within European marine waters. It is worth noting that eight alien species were reported for the first time in European marine waters and other three were observed outside their known spatial range. This key finding demonstrates the potential of CS in documenting the spread of introduced organisms, especially at small or local scale where traditional scientific information is often lacking and could timely inform management plans aiming to reduce the risk of alien species introduction in new marine habitats.

Several examples highlight the importance of CS in reporting marine alien species worldwide at large and small scales. Approximately 1000 volunteers assessed the presence of the invasive crabs Carcinus maenas and Hemigrapsus sanguineus in the intertidal zone along the eastern coast of the United States (Delaney et al. 2008). Citizens also documented the presence of the Indo-Pacific red lionfish Pterois volitans throughout the northern Gulf of Mexico one to two years earlier and more frequently than the traditional reef fish monitoring programs (Scyphers et al. 2015). The contribution of CS also appeared to be crucial to increase the knowledge on alien species in Hellenic waters, where 14 out of the approximately 240 alien species were reported for the first time through CS (Zenetos et al. 2013), and 31 alien mollusk taxa (72% of the validated marine alien mollusks in Hellenic waters) were first found by amateurs, mostly shell collectors and SCUBA divers/photographers (Crocetta et al. 2017). According to a recent review of the marine alien species recorded in the Saronikos Gulf, Greece, citizen scientists reported 42% out of the total number of alien species records, contributing mostly for the molluskan taxa (24 out of 29 species) (Zenetos et al. 2020). Furthermore, important information on the spread of comb jellies was provided by citizens in the context of “Jellywatch,” a Mediterranean Science Commission initiative (Boero et al. 2009). In the same region, CS contributed significantly in alerting on invasive species such as L. sceleratus (Zenetos et al. 2015). Citizens were also effectively involved in monitoring the spread dynamics of the invasive seaweed Caulerpa cylindracea within the Marine Protected Area of Egadi Islands (Mannino and Balistreri 2018).

Another key finding of the present study is that the distribution patterns of CS records of the targeted alien taxa varied among the European marine subregions, a parameter that should be considered in the evaluation of monitoring efforts of marine IAS. In the case of alien fishes, the highest number of CS individual records was found in the Mediterranean Sea and mainly in MAL, while most of the CS records of alien mollusks came from the NE Atlantic and mainly ANS. This heterogeneity may reflect differences in the coastline length and monitoring efforts of each country (Tsiamis et al. 2019). Indeed, the highest number of CS records of alien fishes was found in Greece, a country with the second largest coastline (13,676 km) in Europe and the majority of CS initiatives/scientific projects within the Mediterranean Sea (after France, MWE). The same pattern was observed for mollusks in the United Kingdom that has the second largest coastline (12,429 km) in Europe and where the majority of CS initiatives/scientific projects was recorded within the northeastern Atlantic Ocean. Available funding of CS projects and also how well evolved is the concept of CS in some countries compared to others may also affect the number of alien species recorded by citizens. As stated by Beck et al. (2014), although GBIF is a useful tool in mapping alien species, by integrating the georeferenced data uploaded in other different open platforms, the distribution data may be spatially biased given to the nation-wide differences in funding and data sharing. This is well depicted by Thiel et al. (2014) who show that CS in the marine environment is still an infrequently used approach in developing countries.

Assessing the distribution of CS records of alien fishes in time revealed a gradual increase in numbers of individuals and new species during the last decade in all European marine waters, especially in the eastern Mediterranean Sea (MAL). This could be attributed to the well-documented acceleration of successful introductions of alien species from the Red Sea (Ben Rais Lasram and Mouillot 2009, Zenetos et al. 2012, Katsanevakis et al. 2013, Galil et al. 2014), and also to the recent growth of CS projects and the use of smartphone applications combined with social media (Miller-Rushing et al. 2012, Cappa et al. 2016, Johnson et al. 2020).

The number of CS records of marine alien species may also be connected to their biological/morphological features, their invasive behavior, and the extent of their geographical distribution. This becomes evident in the case of the Indo-Pacific originated L. sceleratus, the most reported species by citizens in the Mediterranean Sea and specifically in Greece (57.03%) and Italy (35.74%). This pufferfish is considered one of the fastest expanding invasive species in the Mediterranean basin (Akyol et al. 2005) due to its high growth and reproduction rates, the lack of natural predators, the ability to exploit food resources, and its environmental plasticity (Yaglioglu et al. 2011). These biological features, combined with the vicinity of the Aegean-Levantine Sea to the marine area of the species native origin, have made L. sceleratus one of the most abundant alien pufferfishes in the eastern Mediterranean Sea. Additionally, it can be easily tracked, identified, and reported by citizens, because it is a large and conspicuous fish. Large and easily identified fishes are also P. miles and F. commersonii that were the second and third most reported species by citizens in our study. Their high reproductive rate coupled with the lack of natural predators have significantly enhanced their expansion in the Mediterranean Sea (Azzurro et al. 2014, Kleitou et al. 2016). It should be also noted that another possible reason for high reporting is that more people are interested in fishes by hobby than in other marine organisms, a fact that increases the alien fishes recorded by citizens. The fact that the total number of fish species recorded in European marine waters is 160 (according to EASIN), of which 71 were reported through CS (46.88%), while the total number of mollusks recorded is 228, of which 72 were reported through CS (32.02%), could support the notion that people are more prone to look for/identify different fish species than other marine taxa.

Citizen science records of alien mollusks in European marine waters also showed a significant increase during the last decade in terms of number of individuals in the NE Atlantic, mainly in ANS, and number of species in the Mediterranean Sea, mainly in MAL. A peak was observed between 2013 and 2017. Among mollusks, the highest percentage belonged to the slipper limpet C. fornicata, which was mostly recorded in ANS (78.81%) among all MSFD subregions. Crepidula fornicata, originating from NW Atlantic, was first introduced into the European coastal waters in the 1880s/1890s, attached to the American wellfleet oyster Crassostrea virginica that was imported into the United Kingdom for aquaculture purposes at that time (Bohn et al. 2015 and references therein). Its ability to colonize most natural and manmade hard substrata and to thrive in a variety of environmental conditions (Loomis and Van Nieuwenhuyze 1985) has resulted in its repeated accidental introduction by being attached to ships, wreckage, and, especially, transported shellfish species (Bohn et al. 2015 and references therein). After its initial establishment, it quickly spread in the North, Celtic, and Baltic seas, and today, its densities in the coastal waters of the United Kingdom and France often exceed 1000 individuals/m² (FitzGerald 2007). This in combination with the fact that the United Kingdom is among the most active countries in terms of marine CS projects (Thiel et al. 2014) could explain that 81.78% of all CS records of C. fornicata were found in this country. Only 14 records of the species were reported by citizens in the Mediterranean (Greece, MAL; Spain, MWE). According to Blanchard (1997), several records of C. fornicata come from the Mediterranean Sea, but they are restricted to a few areas of intensive oyster and mussel culture (Blanchard 1997). Similarly to C. fornicata, the false angel wing P. pholadiformis, which is native to the NW Atlantic, was introduced into the Southern United Kingdom in early 1890s, mainly through the accidental transport with the Crassostrea oysters and ballast water discharge. Since then, the species has colonized the marine waters of several Northern European countries and today is well established in Belgium, Germany, Denmark, Norway, the Netherlands, Sweden, and the United Kingdom (NOBANIS 2020). The wide species distribution in the NE Atlantic is witnessed by the fact that 99.10% of all CS records of P. pholadiformis in European marine waters were found in the ANS, and mainly in the Netherlands (37.87%), Belgium (34.53%), and Germany (23.75%).

Citizen science is centered on the discovery of the socio-scientific outcomes of expert/non-expert partnerships that involve collecting authentic scientific data (Jordan et al. 2015). Different theoretical frameworks have been proposed to describe the nature of CS participation, which may involve either individuals guided by scientific experts or individuals who participate in the entire scientific process and are not limited to data collection only (Bonney et al. 2009b, Shirk et al. 2012). Our results showed that most of the CS records (79%) were collected by volunteers who were engaged in scientific projects or initiatives. The rest of the CS data were reported in forums (e.g., “seawatchers,” “iNaturalist Research-grade Observations,” “Diveboard—Scuba diving citizen science observations,”). In both cases, the participation of citizens was limited to data collection only, despite the potential of citizens to undertake all aspects of the scientific study after adopting requisite expertise and qualifications (Jordan et al. 2015). According to Shirk et al. (2012), the more the public is involved in the entire scientific process and extends beyond data collection and analysis, the more a project affects the outcomes in learning and science literacy, which may be further linked to outcomes at community level (Jordan et al. 2015). In the context of maximizing these outcomes, a greater level of participation that enhances individual science identity and personal agency should be encouraged.

The contribution of CS to increase our current knowledge on alien species distribution is unquestionable (Zenetos et al. 2013, Theobald et al. 2015, Mannino and Balistreri 2018, Johnson et al. 2020). Nevertheless, the variable educational or professional background of citizens poses particular challenges for the professional scientists who are called to transfer the skills and norms to collect data of scientific quality to the public (Thiel et al. 2014). Often the scientific community seems reluctant to trust the data generated through CS due to the lack of certification of their validity (Delaney et al. 2008), which may limit the “scaling up” of CS, namely, its extension in terms of both, the number of participants and the geographic extent (Maccani et al. 2020), and consequently the impact of CS research. The validation of CS data following rigorous scientific methodology is necessary for their acceptance by the scientific community and stakeholders (Boudreau and Yan 2004). During recent years, there have been significant efforts in this direction, specifically in evaluating the accuracy and validity of the generated CS data (Thiel et al. 2014) apart from engaging citizens in scientific projects (Zenetos et al. 2013, Theobald et al. 2015). This was also depicted in our study where the vast majority (88.51%) of the CS records concerning the targeted groups were validated by scientific experts, even though only for few validated records (15.8%) a picture was available in the final web interfaces. This finding highlights the potential of CS data to be integrated/included in decision-making processes after proper scientific curation, and even further following a close collaboration with scientists during field observations. This interaction is expected to increase the scalability and spreading of CS initiatives beyond their particular local context, an issue that still remains challenging. Thus, all perspectives of maximizing the accuracy and validity of the scientific data should be considered in CS research.

Marine alien species are being introduced into the European seas at an alarming rate, and the creation of public awareness campaigns seems more urgent than ever in view of the significant role that CS may have in the management of alien species introductions. Our findings suggest that CS with proper scientific guidance plays a key role in understanding the distribution patterns of marine alien fishes and mollusks and their ecological effect on global marine biodiversity. The engagement of citizens in scientific monitoring programs on alien species would allow the development and implementation of more effective management strategies at European level, considering the vast quantity of data generated at large time and space scales. This is facilitated by the rapid growth and increasing popularity of smartphone technology and sophisticated data collection tools, which are becoming more and more available to citizens. Taking advantage of the smartphone-based applications, the effective video-training that citizens can remotely get (Starr et al. 2014) and proper verification protocols, accurate data can be collected in a cost-effective way providing substantial complementary information on species distribution, population abundance, and biological traits. Such information could contribute to the assessment of the MSFD Descriptor 2 (non-indigenous species; EC 2008) and could support the effective implementation of the IAS Regulation.

Acknowledgments

This study has been accomplished in the frame of the Short-Term Scientific Mission (STSM) of Dr. Vasiliki Kousteni that took place in the Directorate for Sustainable Resources (Water and Marine Resources Unit), in the Joint Research Centre (JRC, Ispra, Italy), and has been funded by the Cost Action CA17122—Increasing Understanding of Alien Species through Citizen Science (https://www.cost.eu/actions/CA17122/#).